GM-CSF alters dendritic cells in autoimmune diseases

Autoimmunity

Volumn 46, Issue 7, 2013, Pages 409-418

  Li, Bao Zhu ^a   Ye, Qian Ling ^b   Xu, Wang Dong ^a   Li, Jie Hua ^a   Ye, Dong Qing ^a   Xu, Yuekang ^c  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b Department of Infectious Diseases   (China)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Autoimmune diseases; Dendritic cells; GM CSF; Immune regulation; Inflammation

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR ANTIBODY; METHOTREXATE; MONOCLONAL ANTIBODY; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ARTICLE; ASTHMA; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CLINICAL TRIAL; DENDRITIC CELL; HUMAN; IMMUNITY; MONOCYTE; MULTIPLE SCLEROSIS; NONHUMAN; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; THYMUS;

ANIMALS; AUTOIMMUNE DISEASES; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; INFLAMMATION MEDIATORS; LYMPHOCYTE SUBSETS; LYMPHOID TISSUE; STEM CELLS;

EID: 84885442341     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2013.803533     Document Type: Article

References (115)

1. Metcalf, D. 2008. Hematopoietic cytokines. Blood. 111: 485-491.
2. Greter, M., J. Helft, A. Chow, D. Hashimoto, A. Mortha, J. Agudo-Cantero, M. Bogunovic, et al. 2012. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity. 36: 1031-1046.
3. Burgess, A. W., J. Camakaris, and D. Metcalf. 1977. Purification and properties of colony-stimulating factor from mouse lungconditioned medium. J Biol Chem. 252: 1998-2003. (Pubitemid 8077588)
4. Metcalf, D. 1986. The molecular biology and functions of the granulocyte-macrophage colony-stimulating factors. Blood. 67: 257-267. (Pubitemid 16164633)
5. Zhan, Y., Y. Xu, and A. M. Lew. 2012. The regulation of the development and function of dendritic cell subsets by GMCSF: more than a hematopoietic growth factor. Mol Immunol. 52: 30-37.
6. Campbell, I. K., A. van Nieuwenhuijze, E. Segura, K. O'Donnell, E. Coghill, M. Hommel, S. Gerondakis, et al. 2011. Differentiation of inflammatory dendritic cells is mediated by NF-kappaB1-dependent GM-CSF production in CD4 T cells. J Immunol. 186: 5468-5477.
7. Wodnar-Filipowicz, A., C. H. Heusser, and C. Moroni. 1989. Production of the haemopoietic growth factors GM-CSF and interleukin-3 by mast cells in response to IgE receptor-mediated activation. Nature. 339: 150-152. (Pubitemid 19122273)
8. Lenhoff, S., B. Sallerfors, and T. Olofsson. 1998. IL-10 as an autocrine regulator of CSF secretion by monocytes: disparate effects on GM-CSF and G-CSF secretion. Exp Hematol. 26: 299-304. (Pubitemid 28177787)
9. Le, P. T., S. Lazorick, L. P. Whichard, Y. C. Yang, S. C. Clark, B. F. Haynes, and K. H. Singer. 1990. Human thymic epithelial cells produce IL-6, granulocyte-monocyte-CSF, and leukemia inhibitory factor. J Immunol. 145: 3310-3315.
10. Broudy, V. C., K. Kaushansky, J. M. Harlan, and J. W. Adamson. 1987. Interleukin 1 stimulates human endothelial cells to produce granulocyte- macrophage colony-stimulating factor and granulocyte colony-stimulating factor. J Immunol. 139: 464-468. (Pubitemid 17104045)
11. Nimer, S. D., M. J. Gates, H. P. Koeffler, and J. C. Gasson. 1989. Multiple mechanisms control the expression of granulocytemacrophage colony-stimulating factor by human fibroblasts. J Immunol. 143: 2374-2377. (Pubitemid 19245212)
12. Plenz, G., S. Reichenberg, C. Koenig, J. Rauterberg, M. C. Deng, H. A. Baba, and H. Robenek. 1999. Granulocyte-macrophage colony-stimulating factor (GM-CSF) modulates the expression of type VIII collagen mRNA in vascular smooth muscle cells and both are codistributed during atherogenesis. Arterioscler Thromb Vasc Biol. 19: 1658-1668. (Pubitemid 29323824)
13. Djoumerska-Alexieva, I., S. Pashova, T. Vassilev, and A. Pashov. 2013. The protective effect of modified intravenous immunoglobulin in LPS sepsis model is associated with an increased IRA B cells response. Autoimmun Rev. 12: 653-656.
14. Hansen, G., T. R. Hercus, B. J. McClure, F. C. Stomski, M. Dottore, J. Powell, H. Ramshaw, et al. 2008. The structure of the GM-CSF receptor complex reveals a distinct mode of cytokine receptor activation. Cell. 134: 496-507.
15. Dhar-Mascareno, M., J. Chen, R. H. Zhang, J. M. Carcamo, and D. W. Golde. 2003. Granulocyte-macrophage colony-stimulating factor signals for increased glucose transport via phosphatidylinositol 3-kinase-and hydrogen peroxide-dependent mechanisms. J Biol Chem. 278: 11107-11114. (Pubitemid 36792663)
16. Hayashida, K., T. Kitamura, D. M. Gorman, K. Arai, T. Yokota, and A. Miyajima. 1990. Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor. Proc Natl Acad Sci USA. 87: 9655-9659. (Pubitemid 120016501)
17. McClure, B. J., T. R. Hercus, B. A. Cambareri, J. M. Woodcock, C. J. Bagley, G. J. Howlett, and A. F. Lopez. 2003. Molecular assembly of the ternary granulocyte-macrophage colony-stimulating factor receptor complex. Blood. 101: 1308-1315. (Pubitemid 36182500)
18. Kitamura, T., N. Sato, K. Arai, and A. Miyajima. 1991. Expression cloning of the human IL-3 receptor cDNA reveals a shared beta subunit for the human IL-3 and GM-CSF receptors. Cell. 66: 1165-1174. (Pubitemid 121001406)
19. Hamilton, J. A., and G. P. Anderson. 2004. GM-CSF biology. Growth Factors. 22: 225-231. (Pubitemid 40123401)
20. van de Laar, L., P. J. Coffer, and A. M. Woltman. 2012. Regulation of dendritic cell development by GM-CSF: molecular control and implications for immune homeostasis and therapy. Blood. 119: 3383-3393.
21. Meads, M. B., Z. W. Li, and W. S. Dalton. 2010. A novel TNF receptor-associated factor 6 binding domain mediates NF-kappa B signaling by the common cytokine receptor beta subunit. J Immunol. 185: 1606-1615.
22. Sheng, J. R., T. Muthusamy, B. S. Prabhakar, and M. N. Meriggioli. 2011. GM-CSF-induced regulatory T cells selectively inhibit antiacetylcholine receptor-specific immune responses in experimental myasthenia gravis. J Neuroimmunol. 240-241: 65-73.
23. Hamilton, J. A. 2008. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol. 8: 533-544. (Pubitemid 351913679)
24. McQualter, J. L., R. Darwiche, C. Ewing, M. Onuki, T. W. Kay, J. A. Hamilton, H. H. Reid, and C. C. Bernard. 2001. Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J Exp Med. 194: 873-882.
25. Ponomarev, E. D., L. P. Shriver, K. Maresz, J. Pedras-Vasconcelos, D. Verthelyi, and B. N. Dittel. 2007. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J Immunol. 178: 39-48. (Pubitemid 46039660)
26. Carrieri, P. B., V. Provitera, T. De Rosa, G. Tartaglia, F. Gorga, and O. Perrella. 1998. Profile of cerebrospinal fluid and serum cytokines in patients with relapsing-remitting multiple sclerosis: a correlation with clinical activity. Immunopharmacol Immunotoxicol. 20: 373-382. (Pubitemid 28432235)
27. Campbell, I. K., A. Bendele, D. A. Smith, and J. A. Hamilton. 1997. Granulocyte-macrophage colony stimulating factor exacerbates collagen induced arthritis in mice. Ann Rheum Dis. 56: 364-368. (Pubitemid 27305424)
28. Campbell, I. K., M. J. Rich, R. J. Bischof, A. R. Dunn, D. Grail, and J. A. Hamilton. 1998. Protection from collagen-induced arthritis in granulocyte-macrophage colony-stimulating factor-deficient mice. J Immunol. 161: 3639-3644.
29. Cook, A. D., E. L. Braine, I. K. Campbell, M. J. Rich, and J. A. Hamilton. 2001. Blockade of collagen-induced arthritis post-onset by antibody to granulocyte-macrophage colony-stimulating factor (GM-CSF): requirement for GM-CSF in the effector phase of disease. Arthritis Res. 3: 293-298. (Pubitemid 32821522)
30. Campbell, I. K., M. J. Rich, R. J. Bischof, and J. A. Hamilton. 2000. The colony-stimulating factors and collagen-induced arthritis: exacerbation of disease by M-CSF and G-CSF and requirement for endogenous M-CSF. J Leukoc Biol. 68: 144-150.
31. Xu, W. D., G. S. Firestein, R. Taetle, K. Kaushansky, and N. J. Zvaifler. 1989. Cytokines in chronic inflammatory arthritis. II. Granulocyte-macrophage colony-stimulating factor in rheumatoid synovial effusions. J Clin Invest. 83: 876-882. (Pubitemid 19080619)
32. Hazenberg, B. P., M. A. Van Leeuwen, M. H. Van Rijswijk, A. C. Stern, and E. Vellenga. 1989. Correction of granulocytopenia in Felty's syndrome by granulocyte-macrophage colony-stimulating factor. Simultaneous induction of interleukin-6 release and flare-up of the arthritis. Blood. 74: 2769-2770. (Pubitemid 20007805)
33. Noguchi, M., N. Hiwatashi, Z. X. Liu, and T. Toyota. 2001. Increased secretion of granulocyte-macrophage colony-stimulating factor in mucosal lesions of inflammatory bowel disease. Digestion. 63: 32-36. (Pubitemid 32098438)
34. Ina, K., K. Kusugami, T. Hosokawa, A. Imada, T. Shimizu, T. Yamaguchi, M. Ohsuga, et al. 1999. Increased mucosal production of granulocyte colony-stimulating factor is related to a delay in neutrophil apoptosis in Inflammatory Bowel disease. J Gastroenterol Hepatol. 14: 46-53. (Pubitemid 29087317)
35. Gaudreau, S., C. Guindi, M. Menard, G. Besin, G. Dupuis, and A. Amrani. 2007. Granulocyte-macrophage colony-stimulating factor prevents diabetes development in NOD mice by inducing tolerogenic dendritic cells that sustain the suppressive function of CD4\+CD25\+ regulatory T cells. J Immunol. 179: 3638-3647.
36. Enzler, T., S. Gillessen, M. Dougan, J. P. Allison, D. Neuberg, D. A. Oble, M. Mihm, and G. Dranoff. 2007. Functional deficiencies of granulocyte-macrophage colony stimulating factor and interleukin-3 contribute to insulitis and destruction of beta cells. Blood. 110: 954-961. (Pubitemid 47267434)
37. Krakowski, M., R. Abdelmalik, L. Mocnik, T. Krahl, and N. Sarvetnick. 2002. Granulocyte macrophage-colony stimulating factor (GM-CSF) recruits immune cells to the pancreas and delays STZ-induced diabetes. J Pathol. 196: 103-112.
38. Enzler, T., S. Gillessen, J. P. Manis, D. Ferguson, J. Fleming, F. W. Alt, M. Mihm, and G. Dranoff. 2003. Deficiencies of GM-CSF and interferon gamma link inflammation and cancer. J Exp Med. 197: 1213-1219. (Pubitemid 36570077)
39. Vasu, C., R. N. Dogan, M. J. Holterman, and B. S. Prabhakar. 2003. Selective induction of dendritic cells using granulocyte macrophage-colony stimulating factor, but not fms-like tyrosine kinase receptor 3-ligand, activates thyroglobulin-specific CD4\+/CD25\+ T cells and suppresses experimental autoimmune thyroiditis. J Immunol. 170: 5511-5522. (Pubitemid 36617839)
40. Gangi, E., C. Vasu, D. Cheatem, and B. S. Prabhakar. 2005. IL-10-producing CD4\+CD25\+ regulatory T cells play a critical role in granulocyte-macrophage colony-stimulating factor-induced suppression of experimental autoimmune thyroiditis. J Immunol. 174: 7006-7013. (Pubitemid 40705665)
41. Ganesh, B. B., D. M. Cheatem, J. R. Sheng, C. Vasu, and B. S. Prabhakar. 2009. GM-CSF-induced CD11c\+CD8a-dendritic cells facilitate Foxp3\+ and IL-10\+ regulatory T cell expansion resulting in suppression of autoimmune thyroiditis. Int Immunol. 21: 269-282.
42. Mittag, D., A. I. Proietto, T. Loudovaris, S. I. Mannering, D. Vremec, K. Shortman, L. Wu, and L. C. Harrison. 2011. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol. 186: 6207-6217.
43. Look, M., A. Bandyopadhyay, J. S. Blum, and T. M. Fahmy. 2010. Application of nanotechnologies for improved immune response against infectious diseases in the developing world. Adv Drug Deliv Rev. 62: 378-393.
44. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol. 164: 2978-2986. (Pubitemid 30148956)
45. Kurts, C., M. Cannarile, I. Klebba, and T. Brocker. 2001. Dendritic cells are sufficient to cross-present self-antigens to CD8 T cells in vivo. J Immunol. 166: 1439-1442. (Pubitemid 32114619)
46. Iyoda, T., S. Shimoyama, K. Liu, Y. Omatsu, Y. Akiyama, Y. Maeda, K. Takahara, et al. 2002. The CD8\+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med. 195: 1289-1302. (Pubitemid 34564331)
47. Bedoui, S., P. G. Whitney, J. Waithman, L. Eidsmo, L. Wakim, I. Caminschi, R. S. Allan, et al. 2009. Cross-presentation of viral and self antigens by skin-derived CD103\+ dendritic cells. Nat Immunol. 10: 488-495.
48. Belz, G. T., C. M. Smith, D. Eichner, K. Shortman, G. Karupiah, F. R. Carbone, and W. R. Heath. 2004. Cutting edge: conventional CD8 alpha\+ dendritic cells are generally involved in priming CTL immunity to viruses. J Immunol. 172: 1996-2000. (Pubitemid 38182342)
49. Edelson, B. T., T. R. Bradstreet, K. Hildner, J. A. Carrero, K. E. Frederick, W. Kc, R. Belizaire, et al. 2011. CD8alpha(\+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity. 35: 236-248.
50. Onai, N., A. Obata-Onai, M. A. Schmid, T. Ohteki, D. Jarrossay, and M. G. Manz. 2007. Identification of clonogenic common Flt3\+M-CSFR\+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol. 8: 1207-1216. (Pubitemid 350011759)
51. Lande, R., and M. Gilliet. 2010. Plasmacytoid dendritic cells: key players in the initiation and regulation of immune responses. Ann NY Acad Sci. 1183: 89-103.
52. Villadangos, J. A., and L. Young. 2008. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity. 29: 352-361.
53. Merad, M., F. Ginhoux, and M. Collin. 2008. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol. 8: 935-947.
54. King, I. L., M. A. Kroenke, and B. M. Segal. 2010. GM-CSFdependent, CD103\+ dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. J Exp Med. 207: 953-961.
55. Poulin, L. F., S. Henri, B. de Bovis, E. Devilard, A. Kissenpfennig, and B. Malissen. 2007. The dermis contains langerin\+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med. 204: 3119-3131.
56. Helft, J., B. Manicassamy, P. Guermonprez, D. Hashimoto, A. Silvin, J. Agudo, B. D. Brown, et al. 2012. Cross-presenting CD103\+ dendritic cells are protected from influenza virus infection. J Clin Invest. 122: 4037-4047.
57. Shklovskaya, E., B. J. O'Sullivan, L. G. Ng, B. Roediger, R. Thomas, W. Weninger, and B. Fazekas de St Groth. 2011. Langerhans cells are precommitted to immune tolerance induction. Proc Natl Acad Sci USA. 108: 18049-18054.
58. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 19: 59-70. (Pubitemid 36859901)
59. Zhan, Y., and L. Wu. 2012. Functional regulation of monocytederived dendritic cells by microRNAs. Protein Cell. 3: 497-507.
60. Burnham, K., L. Robb, C. L. Scott, M. O'Keeffe, and K. Shortman. 2000. Effect of granulocyte-macrophage colony-stimulating factor on the generation of epidermal Langerhans cells. J Interferon Cytokine Res. 20: 1071-1076. (Pubitemid 32015246)
61. Vremec, D., G. J. Lieschke, A. R. Dunn, L. Robb, D. Metcalf, and K. Shortman. 1997. The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol. 27: 40-44. (Pubitemid 27046056)
62. Egea, L., Y. Hirata, and M. F. Kagnoff. 2010. GM-CSF: a role in immune and inflammatory reactions in the intestine. Expert Rev Gastroenterol Hepatol. 4: 723-731.
63. Shortman, K., and S. H. Naik. 2007. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol. 7: 19-30. (Pubitemid 46020824)
64. Zhan, Y., E. M. Carrington, A. van Nieuwenhuijze, S. Bedoui, S. Seah, Y. Xu, N. Wang, et al. 2011. GM-CSF increases crosspresentation and CD103 expression by mouse CD8(\+) spleen dendritic cells. Eur J Immunol. 41: 2585-2595.
65. Zhan, Y., J. Vega-Ramos, E. M. Carrington, J. A. Villadangos, A. M. Lew, and Y. Xu. 2012. The inflammatory cytokine, GM-CSF, alters the developmental outcome of murine dendritic cells. Eur J Immunol. 42: 2889-2900.
66. Esashi, E., Y. H. Wang, O. Perng, X. F. Qin, Y. J. Liu, and S. S. Watowich. 2008. The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity. 28: 509-520.
67. Xu, Y., Y. Zhan, A. M. Lew, S. H. Naik, and M. H. Kershaw. 2007. Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol. 179: 7577-7584.
68. Gilliet, M., A. Boonstra, C. Paturel, S. Antonenko, X. L. Xu, G. Trinchieri, A. O'Garra, and Y. J. Liu. 2002. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colonystimulating factor. J Exp Med. 195: 953-958. (Pubitemid 34286765)
69. McLellan, A. D., M. Kapp, A. Eggert, C. Linden, U. Bommhardt, E. B. Brocker, U. Kammerer, and E. Kampgen. 2002. Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression. Blood. 99: 2084-2093. (Pubitemid 34525492)
70. Vremec, D., and K. Shortman. 1997. Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J Immunol. 159: 565-573. (Pubitemid 127484204)
71. Dresch, C., M. Ackermann, B. Vogt, B. de Andrade Pereira, K. Shortman, and C. Fraefel. 2011. Thymic but not splenic CD8(\+) DCs can efficiently cross-prime T cells in the absence of licensing factors. Eur J Immunol. 41: 2544-2555.
72. Rapin, N., E. Mosekilde, and O. Lund. 2011. Bistability in autoimmune diseases. Autoimmunity. 44: 256-260.
73. Schmidt, S. V., A. C. Nino-Castro, and J. L. Schultze. 2012. Regulatory dendritic cells: there is more than just immune activation. Front Immunol. 3: 274.
74. Kis-Toth, K., and G. C. Tsokos. 2010. Dendritic cell function in lupus: Independent contributors or victims of aberrant immune regulation. Autoimmunity. 43: 121-130.
75. Mayer, C. T., L. Berod, and T. Sparwasser. 2012. Layers of dendritic cell-mediated T cell tolerance, their regulation and the prevention of autoimmunity. Front Immunol. 3: 183.
76. Platt, C. D., J. K. Ma, C. Chalouni, M. Ebersold, H. Bou-Reslan, R. A. Carano, I. Mellman, and L. Delamarre. 2010. Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci USA. 107: 4287-4292.
77. Volkmann, A., T. Zal, and B. Stockinger. 1997. Antigen-presenting cells in the thymus that can negatively select MHC class IIrestricted T cells recognizing a circulating self antigen. J Immunol. 158: 693-706. (Pubitemid 127492647)
78. O'Garra, A., and P. Vieira. 2007. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol. 7: 425-428. (Pubitemid 46834852)
79. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu Rev Immunol. 18: 767-811. (Pubitemid 30365397)
80. Land, W. G. 2005. Injury to allografts: innate immune pathways to acute and chronic rejection. Saudi J Kidney Dis Transpl. 16: 520-539. (Pubitemid 43123428)
81. Janikashvili, N., B. Bonnotte, E. Katsanis, and N. Larmonier. 2011. The dendritic cell-regulatory T lymphocyte crosstalk contributes to tumor-induced tolerance. Clin Dev Immunol. 2011: 430394.
82. Conti, L., and S. Gessani. 2008. GM-CSF in the generation of dendritic cells from human blood monocyte precursors: recent advances. Immunobiology. 213: 859-870.
83. Torres-Aguilar, H., M. Blank, L. J. Jara, and Y. Shoenfeld. 2010. Tolerogenic dendritic cells in autoimmune diseases: crucial players in induction and prevention of autoimmunity. Autoimmun Rev. 10: 8-17.
84. Lutz, M. B., N. A. Kukutsch, M. Menges, S. Rossner, and G. Schuler. 2000. Culture of bone marrow cells in GM-CSF plus high doses of lipopolysaccharide generates exclusively immature dendritic cells which induce alloantigen-specific CD4 T cell anergy in vitro. Eur J Immunol. 30: 1048-1052. (Pubitemid 30216220)
85. Menges, M., S. Rossner, C. Voigtlander, H. Schindler, N. A. Kukutsch, C. Bogdan, K. Erb, et al. 2002. Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J Exp Med. 195: 15-21. (Pubitemid 34074492)
86. Gross, C. C., H. Jonuleit, and H. Wiendl. 2012. Fulfilling the dream: tolerogenic dendritic cells to treat multiple sclerosis. Eur J Immunol. 42: 569-572.
87. Zou, Y. F., X. L. Feng, F. M. Pan, H. Su, J. H. Tao, and D. Q. Ye. 2010. Meta-analysis of TNF-alpha promoter-238A/G polymorphism and SLE susceptibility. Autoimmunity 43: 264-274.
88. Kanauchi, H., F. Furukawa, and S. Imamura. 1989. Evaluation of ATPase-positive Langerhans' cells in skin lesions of lupus erythematosus and experimentally induced inflammations. Arch Dermatol Res. 281: 327-332. (Pubitemid 19222016)
89. Crispin, J. C., M. I. Vargas-Rojas, A. Monsivais-Urenda, and J. Alcocer-Varela. 2012. Phenotype and function of dendritic cells of patients with systemic lupus erythematosus. Clin Immunol. 143: 45-50.
90. Scheinecker, C., B. Zwolfer, M. Koller, G. Manner, and J. S. Smolen. 2001. Alterations of dendritic cells in systemic lupus erythematosus: phenotypic and functional deficiencies. Arthritis Rheum. 44: 856-865. (Pubitemid 32319778)
91. Fransen, J. H., L. B. Hilbrands, J. Ruben, M. Stoffels, G. J. Adema, J. van der Vlag, and J. H. Berden. 2009. Mouse dendritic cells matured by ingestion of apoptotic blebs induce T cells to produce interleukin-17. Arthritis Rheum. 60: 2304-2313.
92. Fehr, E. M., S. Spoerl, P. Heyder, M. Herrmann, I. Bekeredjian-Ding, N. Blank, H. M. Lorenz, and M. Schiller. 2012. Apoptoticcell-derived membrane vesicles induce an alternative maturation of human dendritic cells which is disturbed in SLE. J Autoimmun. 40: 86-95.
93. Teh, B. K., J. G. Yeo, L. M. Chern, J. Lu. 2011. C1q regulation of dendritic cell development from monocytes with distinct cytokine production and T cell stimulation. Mol Immunol. 48: 1128-1138.
94. Jongbloed, S. L., M. C. Lebre, A. R. Fraser, J. A. Gracie, R. D. Sturrock, P. P. Tak, and I. B. McInnes. 2006. Enumeration and phenotypical analysis of distinct dendritic cell subsets in psoriatic arthritis and rheumatoid arthritis. Arthritis Res Ther. 8: R15.
95. Thomas, R., L. S. Davis, and P. E. Lipsky. 1994. Rheumatoid synovium is enriched in mature antigen-presenting dendritic cells. J Immunol. 152: 2613-2623. (Pubitemid 24097956)
96. MacDonald, K. P., A. R. Pettit, C. Quinn, G. J. Thomas, and R. Thomas. 1999. Resistance of rheumatoid synovial dendritic cells to the immunosuppressive effects of IL-10. J Immunol. 163: 5599-5607.
97. Lebre, M. C., and P. P. Tak. 2008. Dendritic cell subsets: their roles in rheumatoid arthritis. Acta Rheumatol Port. 33: 35-45.
98. Radstake, T. R., P. L. van Lent, G. J. Pesman, A. B. Blom, F. G. Sweep, J. Ronnelid, G. J. Adema, et al. 2004. High production of proinflammatory and Th1 cytokines by dendritic cells from patients with rheumatoid arthritis, and down regulation upon FcgammaR triggering. Ann Rheum Dis. 63: 696-702. (Pubitemid 38658400)
99. Roelofs, M. F., L. A. Joosten, S. Abdollahi-Roodsaz, A. W. van Lieshout, T. Sprong, F. H. van den Hoogen, W. B. van den Berg, and T. R. Radstake. 2005. The expression of toll-like receptors 3 and 7 in rheumatoid arthritis synovium is increased and costimulation of toll-like receptors 3, 4, and 7/8 results in synergistic cytokine production by dendritic cells. Arthritis Rheum. 52: 2313-2322. (Pubitemid 41117415)
100. Tsark, E. C., W. Wang, Y. C. Teng, D. Arkfeld, G. R. Dodge, and S. Kovats. 2002. Differential MHC class II-mediated presentation of rheumatoid arthritis autoantigens by human dendritic cells and macrophages. J Immunol. 169: 6625-6633. (Pubitemid 36903517)
101. Karman, J., H. H. Chu, D. O. Co, C. M. Seroogy, M. Sandor, and Z. Fabry. 2006. Dendritic cells amplify T cell-mediated immune responses in the central nervous system. J Immunol. 177: 7750-7760. (Pubitemid 44846291)
102. Sun, Y., I. Peng, K. Senger, K. Hamidzadeh, M. Reichelt, M. Baca, R. Yeh, et al. 2013. Critical role of activation induced cytidine deaminase in experimental autoimmune Encephalomyelitis. Autoimmunity. 46: 157-167.
103. Greter, M., F. L. Heppner, M. P. Lemos, B. M. Odermatt, N. Goebels, T. Laufer, R. J. Noelle, and B. Becher. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med. 11: 328-334. (Pubitemid 40460562)
104. Karni, A., M. Abraham, A. Monsonego, G. Cai, G. J. Freeman, D. Hafler, S. J. Khoury, and H. L. Weiner. 2006. Innate immunity in multiple sclerosis: myeloid dendritic cells in secondary progressive multiple sclerosis are activated and drive a proinflammatory immune response. J Immunol. 177: 4196-4202. (Pubitemid 44359955)
105. Huang, Y. M., B. G. Xiao, V. Ozenci, M. Kouwenhoven, N. Teleshova, S. Fredrikson, and H. Link. 1999. Multiple sclerosis is associated with high levels of circulating dendritic cells secreting pro-inflammatory cytokines. J Neuroimmunol. 99: 82-90. (Pubitemid 29488572)
106. King, I. L., T. L. Dickendesher, and B. M. Segal. 2009. Circulating Ly-6C\+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood. 113: 3190-3197.
107. Mausberg, A. K., S. Jander, and G. Reichmann. 2009. Intracerebral granulocyte-macrophage colony-stimulating factor induces functionally competent dendritic cells in the mouse brain. Glia. 57: 1341-1350.
108. Hesske, L., C. Vincenzetti, M. Heikenwalder, M. Prinz, W. Reith, A. Fontana, and T. Suter. 2010. Induction of inhibitory central nervous system-derived and stimulatory blood-derived dendritic cells suggests a dual role for granulocyte-macrophage colonystimulating factor in central nervous system inflammation. Brain. 133: 1637-1654.
109. Burmester, G. R., E. Feist, M. A. Sleeman, B. Wang, B. White, and F. Magrini. 2011. Mavrilimumab, a human monoclonal antibody targeting GM-CSF receptor-alpha, in subjects with rheumatoid arthritis: a randomised, double-blind, placebo-controlled, phase I, first-in-human study. Ann Rheum Dis. 70: 1542-1549.
110. Burmester, G. R., M. E. Weinblatt, I. B. McInnes, D. Porter, O. Barbarash, M. Vatutin, I. Szombati, et al. 2012. Efficacy and safety of mavrilimumab in subjects with rheumatoid arthritis. Ann Rheum Dis [Epub ahead of print].
111. ClinicalTrials.gov. Information provided by MorphoSys AG. http://clinicaltrials.gov/ct2/show/NCT01023256?term=MOR +103&rank=1 (Accessed January 20, 2013).
112. ClinicalTrials.gov. Information provided by MorphoSys AG. http://clinicaltrials.gov/ct2/show/NCT01517282?term=MOR +103&rank=2 (Accessed January 20, 2013).
113. ClinicalTrials.gov. Information provided by KaloBios Pharmaceuticals. http://clinicaltrials.gov/ct2/show/NCT00995449 ?term=KB003&rank=2 (Accessed January 20, 2013).
114. ClinicalTrials.gov. Information provided by KaloBios Pharmaceuticals. http://clinicaltrials.gov/ct2/show/NCT01603277 ?term=KB003&rank=1 (Accessed January 20, 2013).
115. Tazawa, R., B. C. Trapnell, Y. Inoue, T. Arai, T. Takada, Y. Nasuhara, N. Hizawa, et al. 2010. Inhaled granulocyte/macrophage-colony stimulating factor as therapy for pulmonary alveolar proteinosis. Am J Respir Crit Care Med. 181: 1345-1354.